The effect of fungal endophytes on thrips and tospovirus epidemiology

Abstract

Onion thrips, Thrips tabaci Lindeman are one of the key pests of onion, Allium cepa L., an economically important agricultural crop cultivated worldwide. Thrips are commonly managed through indiscriminate application of synthetic pesticides. However, most of these pesticides can lead to serious environmental hazards and are ineffective due to a number of factors including development of resistance, pest presence in cryptic habitats and overlapping generations. To remain effective, control programmes have to integrate several pest and disease management tactics including the use of beneficial micro-organisms like endophytic fungi that stimulate the plant defence responses. Endophytic fungi in recent evidence suggest that they can play symbiotic roles in nature, such as antagonists of plant pests and diseases, increased drought tolerance and plant-growth. However, information on endophyte colonization of onions and their impacts on the biology of onion thrips, influence on thrips behaviour and on induction of resistance against thrips and virus replication are lacking. Therefore, the objectives of this study were to determine, (1) colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci, (2) behavioral responses of T. tabaci to endophyte inoculated onion plants, and (3) if endophytic colonization of onions induces resistance against thrips and virus replication. Colonization of onion plants by selected fungal endophyte isolates was tested using two inoculation methods whilst evaluating their effects on biology of T. tabaci. Seven fungal endophytes used in our study were able to colonize onion plants either by the seed or seedling inoculation methods. Seed inoculation resulted in 1.47 times higher mean percentage post inoculation recovery of all the endophytes tested as compared to seedling inoculation. Fewer thrips were observed on plants inoculated with Clonostachys rosea ICIPE 707, Trichoderma asperellum M2RT4, Trichoderma atroviride ICIPE 710, Trichoderma harzianum 709, Hypocrea lixii F3ST1 and Fusarium sp. ICIPE 712 isolates as compared to those inoculated with Fusarium sp. ICIPE 717 and the control. Onion plants colonized by C. rosea ICIPE 707, T. asperellum M2RT4, T. atroviride ICIPE 710 and H. lixii F3ST1 had significantly lower feeding punctures as compared to the other treatments while the lowest numbers of eggs were laid by T. tabaci on H. lixii F3ST1 and C. rosea ICIPE 707 inoculated plants. To study behavior of thrips on endophytically colonized onion plants, choice experiments were conducted in a screen house and the laboratory. Female T. tabaci preferred endophyte- free (E-) over endophyte-inoculated (E+) plants. The number of feeding punctures and eggs were more on E- than on E+ plants. Oviposition was reduced six fold on E+ plants within a 72 h experimental period. In Y-tube olfactometer assay, thrips showed about 3.6 fold preference for E- plants. In individual larval choice experiments, significantly more first-instar and second preferred to feed on leaf sections of E- as compared to the E+ plants. In a settlement preference assay with groups of second-instars, larvae preferred leaf sections from E- over E+ plants with incremental time. To study the effect of endophytic colonization of onions on induced resistance against thrips and virus replication, we conducted screenhouse trials in which a colony of viruliferous thrips were studied for feeding and transmission of iris yellow spot virus (IYSV) on E- and E+ onion plants. The numbers of feeding punctures were significantly lower in E+ as compared to the E- plants. Disease level sampled weekly for four weeks following thrips exposure was significantly lower in E+ as compared to E- plants. IYSV transmission was reduced 2.5-fold by the endophytic fungus on both whole plant and leaf disc assays. Our results suggest potential utility of endophytes to colonize and confer protection on onion plants against thrips damage and virus infection. Further studies should be conducted to determine whether such endophyte-mediated protection against thrips in onion extends to other agricultural crops.